|Year : 2014 | Volume
| Issue : 4 | Page : 945-950
Primary extranodal non-Hodgkin's lymphoma of oral cavity - A single centre retrospective study
Nagesh T Sirsath1, KC Lakshmaiah1, Umesh Das1, D Lokanatha1, S Premlatha Chennagiri2, Clementina Ramarao2
1 Department of Medical Oncology, Kidwai Memorial Institute of Oncology, Banglore, Karnataka, India
2 Department of Pathology, Kidwai Memorial Institute of Oncology, Banglore, Karnataka, India
|Date of Web Publication||9-Jan-2015|
Dr. Umesh Das
Room no. 102, PG Hostel, Kidwai Memorial Institute of Oncology, M.H. Mari Gowda Road, Banglore - 560 029, Karnataka
Source of Support: None, Conflict of Interest: None
Background: Extra nodal involvements of non-Hodgkin's lymphomas (NHL) are not so uncommon, but the involvement of oral cavity by NHL is very rare.
Materials and Methods: The present study involved retrospective analysis of patients from year 2001 to 2011, who presented with oral mass and on evaluation were diagnosed to have primary extranodal NHL of oral cavity at a tertiary cancer care centre in South India.
Results: There were seven patients treated for primary NHL of oral cavity at our institute in last 10 years. The median age at presentation was 43.2 years (range 29-65 years). There were five males and two females. Oral tongue was the most common site (three patients) followed by alveolus (two patients). The other sites of involvement included gingivobuccal sulcus in one patient and hard palate in one patient. All patients were initially evaluated at oral oncology department for gradually increasing ulcerative mass in oral cavity. None of the patients had B symptoms. In our study, plasmablastic lymphoma was the most common type of NHL, followed by diffuse large B cell lymphoma (DLBCL) and peripheral T cell lymphoma, not otherwise specified (PTCL, NOS). Out of seven patients, two were HIV positive, both having plasmablastic lymphoma. Four out of the seven patients received a combination of chemotherapy and radiotherapy and three patients received only chemotherapy. Only three patients could complete the prescribed chemotherapy and radiotherapy schedule and were alive and diseases free with a median follow-up of 21 months.
Conclusion: Involvement of oral cavity by lymphoma is rare. Plasmablastic lymphoma was the most common oral cavity NHL in our patients. Although number of cases in present study was less, our data suggests that oral NHL has aggressive course with less favorable outcome. Further large sample studies incorporating rituximab-based chemotherapy and more aggressive chemotherapy for plasmablastic lymphoma will be helpful for better understanding of treatment outcome.
Keywords: Extranodal, non-Hodgkin′s lymphoma, oral cavity
|How to cite this article:|
Sirsath NT, Lakshmaiah K C, Das U, Lokanatha D, Chennagiri S P, Ramarao C. Primary extranodal non-Hodgkin's lymphoma of oral cavity - A single centre retrospective study. J Can Res Ther 2014;10:945-50
|How to cite this URL:|
Sirsath NT, Lakshmaiah K C, Das U, Lokanatha D, Chennagiri S P, Ramarao C. Primary extranodal non-Hodgkin's lymphoma of oral cavity - A single centre retrospective study. J Can Res Ther [serial online] 2014 [cited 2020 Aug 9];10:945-50. Available from: http://www.cancerjournal.net/text.asp?2014/10/4/945/136024
| > Introduction|| |
Lymphomas are broadly classified as Hodgkin's lymphoma (HL) or non-Hodgkin's lymphoma (NHL).  HL rarely shows extranodal disease (1%) as compared to NHL (25%-30%).  Typical locations of extranodal NHL include gastrointestinal tract, central nervous system, bone, skin, and non-lymphatic structures of head and neck region. Involvement of oral cavity by NHL is very rare. Oral cavity constitutes only 2% of all extranodal lymphomas.  Only a few case reports are available in the literature describing primary extranodal lymphomas of oral cavity. Paucity of available literature because of the rarity of this entity has hindered the progress in understanding the clinical course and subsequent outcomes. The present paper analyses seven cases of primary extranodal lymphomas of oral cavity treated at a tertiary cancer centre in South India along with a detailed review of previously published literature.
| > Materials and Methods|| |
This was a retrospective analysis of patients who presented with oral mass and on evaluation were diagnosed to have for primary NHL lymphoma of oral cavity at a tertiary cancer care centre in South India. The study included patients who were diagnosed and were treated between 2001 and 2011. The diagnosis of oral lymphoma was established by histopathologic examination and immunohistochemistry studies of biopsy specimen. The case files of individual patients were analyzed for information regarding age and gender of patients, site of involvement in oral cavity, clinical staging, international prognostic index (IPI) score, immunohistochemistry report, bone marrow involvement, CNS involvement (including CSF examination), staging CT (neck, thorax, abdomen, and pelvis), and retrovirus positivity status. Treatment modality given, response to treatment, and follow-up status were also analyzed.
| > Results|| |
A total of seven patients were diagnosed as primary oral cavity NHL in last 10 years. The median age at presentation was 43.2 years (range 29-65 years). There were five males and two females. The sites of involvement in oral cavity were oral tongue in three patients, alveolus in two patients, gingivobuccal sulcus in one patient, and hard palate in one patient. All patients presented with gradually increasing ulcerative mass in oral cavity. None of the patients had B symptoms. Bone marrow examination and CSF analysis were done in all patients. None of the patients had bone marrow or CSF involvement. After completion of staging work-up, all the patients fell into stage IE A according to Ann Arbor staging system. All the patients had aggressive NHL. Four patients were diagnosed with plasmablastic lymphoma. Two patients had diffuse large B cell lymphoma (DLBCL). One patient was diagnosed to have peripheral T cell lymphoma, not otherwise specified (PTCL, NOS) of hard palate. On serological testing, two patients were detected to be HIV positive, both had plasmablastic lymphoma (one of oral tongue and the other of alveolus). Four out of the seven patients received a combination of chemotherapy and radiotherapy. Three patients received only chemotherapy; one lost to follow-up after completion of chemotherapy and hence did not receive radiotherapy, one died after first cycle of CVP (cyclophosphamide, vincristine, and prednisolone) chemotherapy, and one died due to progressive disease after three cycles of chemotherapy. CHOP (cyclophosphamide, doxorubicin, vincristine, and prednisolone) was the most commonly used chemotherapy (five patients). Out of the four patients with plasmablastic lymphoma, we had started intensive high-dose chemotherapy in the form of CODOX-M/IVAC protocol (cyclophosphamide, vincristine, doxorubicin, methotrexate, ifosfamide, etoposide, and cytarabine) in a 26-year-old male with plasmablastic lymphoma of right gingivobuccal sulcus; however, he did not tolerate the chemotherapy and later on received palliative radiotherapy. Rest of our plasmablastic lymphoma patients received CHOP chemotherapy. Both HIV-positive patients received intrathecal methotrexate with each cycle of chemotherapy for CNS prophylaxis. CVP was given to the patient with peripheral T cell lymphoma, not otherwise specified (PTCL, NOS) of hard palate in view of low performance score (ECOG 3). Only three patients could complete the prescribed chemotherapy and radiotherapy schedule and were alive and diseases free with a median follow-up of 21 months. 3 patients died during treatment while one patient lost to follow-up [Table 1].
| > Discussion|| |
The oral cavity consists of the lip, floor of mouth, oral tongue (the anterior two thirds of the tongue), buccal mucosa, upper and lower gingiva, hard palate, and retromolar trigone. The incidence of oral cancer is high in India due to high prevalence of tobacco addiction either in the form of smoked tobacco (bidi, cigarettes, chillum, and hookah) or in the form of smokeless tobacco (Gutkha, khaini, and paan masala). It ranks number one in terms of incidence among men and third among women. Age-adjusted rate of oral cancer in India is high that is 20 per 100,000 population and it accounts for over 30% of all cancers in the country.  Almost 95% of oral cavity tumors are squamous cell carcinomas. Primary extranodal lymphoma of oral cavity is very rare. Oral cavity constitutes only 2% of all extranodal lymphomas.  In our study, occurrence of primary extranodal lymphoma of oral cavity was a rare entity with only seven cases encountered over a period of 10 years. Shah et al. have also reported that isolated primary extranodal lymphoma of oral cavity is a rare entity, as they were able to trace only 15 cases of oral NHL over a period of 18 years. 
Van der Waal et al. published the data of 40 cases of primary extranodal NHL of oral cavity.  Median age according to their study was 59 years (3-88 years) and male gander was more commonly affected than female. In the study of Shah et al., the median age of patients with primary extranodal NHL of oral cavity was 46.2 years with M: F ratio of 3:2.  In our study, median age was 43.2 years (range 29-65 years) with a slight male preponderance (five males and two females). Van der Waal et al. have mentioned palate and gingiva as the most common site for oral cavity lymphomas.  In the study of Shah et al. gingivobuccal complex was the site in 12 out of the 15 patients.  In our study, oral tongue was the most common site of oral cavity lymphoma.
In the oral cavity, lymphoma usually presents as an extranodal, soft-elastic, asymptomatic lesion.  Most head and neck NHLs do not have "B" symptoms.  However, Enrique et al. noted B symptoms in 27% patients of head and neck NHL in his series of 31 cases.  In present study, none of the patients had B symptoms and all patients had presented with gradually increasing ulcerative mass in oral cavity. The diagnosis of oral lymphomas may be challenging because frequently there is a low index of clinical suspicion, leading to misdiagnosis and/or delayed treatment. Oral cavity mass can be the rare presentation of a number of conditions including infections such as bacterial osteomyelitis, invasive fungal infection and syphilis, inflammatory diseases particularly Wegener's granulomatosis and neoplasms including squamous cell carcinoma and lymphoma.  Diagnosing the underlying cause requires consideration of several factors as well as gram stain, fungal stain, culture and histopathologic examination of biopsy specimen, and immunohistochemistry studies. 
In immunocompetent individuals, the most common lymphoma in head and neck region is diffuse large cell lymphoma (DLBCL) subtype, although other subtypes of lymphoma like mantle cell lymphoma, marginal zone B-cell lymphoma, Burkitt's lymphoma, lymphomablastic lymphoma, peripheral T-cell lymphoma, and anaplastic large cell lymphoma can also occur.  Hashimoto et al. reviewed pathological characteristics of oral NHL and according to his nine cases and review of literature he concluded that B-cell lymphoma is the most common histological subtype in oral NHL.  In present study, two out of the five immunocompetent patients had DLBCL. According to Teruya-Feldstein et al., the most common histological subtype seen in immunocompromised individuals is plasmablastic variety.  In present study, two patients were detected to be HIV positive, both had plasmablastic lymphoma (one of oral tongue and the other of alveolus). One of the patients was a previously diagnosed case of HIV infection taking antiretroviral treatment for 15 months before lymphoma diagnosis, while the other patient was diagnosed to be seropositive at the time of lymphoma work up. Thus, lymphoma can be the first manifestation of HIV. This has also been reported by other authors. 
HIV is thought to contribute to the development of malignancies through several mechanisms, such as impaired immune surveillance, dysregulation of cytokine pathways and growth factor production, inability to combat genomic instability, chronic B cell stimulation, and imbalance between cellular proliferation and differentiation. More than 80% of lymphomas that occur in HIV-infected patients are high-grade mature B-cell lymphomas,  including both germinal center (GC) and activated B-cell (ABC) subtypes of diffuse large B-cell lymphoma (DLBCL), Burkitt's lymphoma (BL), plasmablastic lymphoma, primary diffuse large B-cell lymphoma of the central nervous system (PCNSL), and primary effusion lymphoma (PEL). By contrast, these histologies make up only 22%-26% of lymphomas in the general population.  Risk of AIDS-related lymphoma is inversely related to CD4 cell count, although the relationship varies among different lymphomas. , Primary CNS lymphomas (PCNSL) often develop in patients with very low CD4 counts (<50/mm 3 ), while GC DLBCL and BLs are generally present in patients with higher CD4 counts. HIV-associated plasmablastic lymphoma has a reported 7:1 male predominance and median CD4 count at diagnosis of 178 cells/mm 3 .  In present study out of two patients of HIV-associated plasmablastic lymphoma, one was male and the other was female and both the patients had CD4 count above 200/mm 3 . In addition to chemotherapy, essential components of an optimal treatment strategy in HIV-associated lymphoma patients include antiretroviral therapy, prophylaxis for opportunistic infections, and rapid recognition and treatment of intercurrent infections. The feasibility of combining chemotherapy with antiretroviral therapy was formally explored in several studies involving CHOP (cyclophosphamide, doxorubicin, vincristine, and prednisone) given with ART. These studies found response rates between 47% and 75%, with a median overall survival (OS) of up to 27 months and OS rates of 58% and 55% at 1 and 2 years, respectively. ,, Consensus exists that rituximab should also be used in CD20-expressing lymphomas in the setting of HIV. Ribera et al.  reported that the complete response rate was 69% with R-CHOP and the estimated three-year OS was 56%. Little et al.  used dose-adjusted EPOCH with ART deferment until chemotherapy completion. They observed 74% complete response rate and 73% two-year progression free survival. There are several practical problems faced while treating these patients. Treatment with ART is complicated by pharmacokinetic drug interactions. Immunodeficiency and cytopenias, common in these patients at the time of initial presentation, are exacerbated by the administration of chemotherapy. Treatment of the malignancy therefore increases the risk of opportunistic infections that, in turn, further compromise the delivery of adequate treatment, which eventually alters treatment outcome. Routine CNS prophylaxis is generally used in AIDS-related lymphomas. Our both patients of HIV-associated lymphoma received CNS prophylaxis in the form of intrathecal methotrexate, with each cycle of chemotherapy along with antiretroviral therapy and Pneumocysis jiroveci prophylaxis.
Median age at presentation of plasmablastic lymphoma is around 50 years and it most frequently presents as mass in the oral cavity, but other extranodal involvement is also seen like paranasal sinus, orbit, skin, bone, soft tissues, and gastrointestinal tract.  Immunophenotypically plasmablastic cells are positive for CD138, CD38, and MUM1. Leukocyte common antigen (LCA) and CD20 positivity uniformly seen in DLBCL cases are usually weak to scant in PBL. Cytoplasmic immunoglobulin, most frequently IgG and either kappa or lambda light chain expression, is seen in 50%-70% of cases. Expression of EMA and CD30 are frequently seen. Ki67 index is usually very high (>90%). In our study, four patients were diagnosed with plasmablastic lymphoma, in all of them CD 138 was positive ki 67 was very high (>90%). The rate of EBV positivity is nearly 100% in oral mucosal plasmablastic lymphoma in HIV-positive cases. HHV8 is consistently absent in plasmablastic lymphoma.  Ann Arbor staging does not appear prognostic, and patients with stage I disease should be treated the same as those with systemic disease.  PBL is characterized by a high proliferative index and aggressive clinical course. Historically, the prognosis has been poor, with median survival less than two years. CHOP has often been used and results are often poor. CODOX-M/IVAC, dose-adjusted EPOCH-like regimens, which are effective in tumor with high proliferative rate, are recommended for treatment of plasmablastic lymphoma. Out of the four patients with plasmablastic lymphoma, we had started intensive high-dose chemotherapy in the form of CODOX-M/IVAC protocol (cyclophosphamide, vincristine, doxorubicin, methotrexate, ifosfamide, etoposide, and cytarabine) in a 26-year-old male with plasmablastic lymphoma of right gingivobuccal sulcus, however he did not tolerate the chemotherapy and later on received palliative radiotherapy. Rest of our plasmablastic lymphoma patients received CHOP chemotherapy. Two patients died during treatment, one patient lost to follow-up after being in complete remission after six cycles of chemotherapy and did not come for radiotherapy. Only one out of the four patients of plasmablastic lymphoma in our study completed the prescribed chemotherapy and radiotherapy schedule and is alive and disease free with a follow-up of 33 months.
Two of our patients had DLBCL. The standard management of DLBCL includes RCHOP with or without radiotherapy. Different regimens of chemotherapy have been proposed in oral NHLs. Maheshwari et al.  used six cycles of CVP regimen, which was followed by radiotherapy of 50 Gy/25 fractions/5 weeks with 19-month disease-free follow-up. Yokobayashi (1981)  used vincristine, epirubicin, and methylprednisolone (VEMP) regimen for his patient; however, patient died after chemotherapy. Shah et al.  have used CHOP chemotherapy, followed by radiotherapy 45 Gy/25 fractions in the management of primary extranodal NHL of oral cavity. Our both DLBCL patients received six cycles of CHOP followed by EBRT 40 Gy/20 fractions. Rituximab was not given due to financial constraints. Both the patients are disease free and are on regular follow-up.
The standard treatment of PTCL, NOS includes CHOP with or without addition of radiotherapy. We had one patient of peripheral T cell lymphoma, not otherwise specified (PTCL, NOS) of hard palate. Our patient received CVP chemotherapy in view of poor performance score. Unfortunately, he died after first cycle of chemotherapy.
According to NCCN guidelines, in selected settings (involvement of paranasal sinuses, testes, bone marrow, HIV lymphomas, ≥2 extranodal sites) CNS prophylaxis should be given with the use of 4-8 doses of intrathecal methotrexate and/or cytarabine during the course of treatment. Both HIV-positive patients in our study received intrathecal methotrexate with each cycle of chemotherapy for CNS prophylaxis.
Chemotherapy, radiotherapy, or both are used in treatment of NHL of head and neck region. Van der Waal et al. used only radiotherapy (28-40 Gy for 2-4 weeks) for stage I oral NHL and combination therapy was used for higher stages.  In his study, chlorambucil with or without prednisolone was used for indolent lymphoma and CHOP was used for aggressive lymphoma. The mortality rate was zero and average survival time for 34 patients was 38 months.  Role of radiotherapy was reviewed by Gustavsson et al. and suggested that combination therapy is needed for aggressive head and neck NHL, but in case of indolent lymphoma only radiation therapy is sufficient as combination therapy did not show any improvement in outcome (after more than 15 year follow-up). 
The survival of extra nodal NHL of head and neck depends on the extent of the disease, presence or absence of HIV serology status, histopathology, and Ann Arbor staging. Five-year survival rate of extra nodal NHL of head and neck was reported by Pazoki et al. and it was 50% and medial survival for stage IE is 10 years.  Wolvius et al. reported 34 cases primary extranodal lymphoma of oral cavity and according to them mean survival time was 38 months with a mean recurrence-free survival time of 31 months.  According to Slootweg et al., survival of oral NHL varies according to Ann Arbor stage and it was 70% for those who presented at base line with stage I disease and 20% for stages II-IV disease.  However, in our study only three patients could complete the prescribed chemotherapy and radiotherapy schedule and are alive and disease free with a median follow-up of 21 months. Three patients died during treatment, while one patient lost to follow-up. Our data suggest that oral NHL has aggressive course with less favorable outcome.
| > Conclusion|| |
Although carcinoma of the oral cavity is very high in our country, the incidence of primary extra nodal NHL is very rare. High-index suspicion is required for diagnosis of this rare disease, as delayed diagnosis ultimately affects the prognosis. Plasmablastic lymphoma was the most common oral cavity NHL in our patients. Our data suggest that oral NHL has aggressive course with less favorable outcome. Our study had limitations in the form that our patients did not receive rituximab due to financial constraints and only one out of the four patients with plasmablastic lymphoma was treated with intensive high-dose chemotherapy. Because of shorter duration of follow-up and small study population, analysis of OS rate was not done in present study. Further large sample studies incorporating rituximab-based chemotherapy and more aggressive chemotherapy for plasmablastic lymphoma will be helpful for understanding the long-term prognosis of this rare entity.
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